Recent sensing technologies for pathogen detection in milk: a review.

Quality control utilising Hazard Analysis and Critical Control Points in the dairy industry generates a large volume of samples. The associated costs are significant. The development and application of fast, sensitive and cost effective analytical systems for pathogen detection in milk could aid the industry in the reduction of overheads, find new uses in dairy farming and production precision management and unlock new markets. Recent progress in pathogen sensing technologies for milk analysis, in particular nucleic acid amplification and biosensors, is reviewed here. The importance of representative samples, detection probability and Practical Detection Limit is clarified. Methods for sample pretreatment are discussed in association with the most applicable detection methods. The major findings are summarised and future perspectives are drawn to inspire new ideas in the scientific community.

[1]  V. Wu,et al.  Using oligonucleotide-functionalized Au nanoparticles to rapidly detect foodborne pathogens on a piezoelectric biosensor. , 2008, Journal of microbiological methods.

[2]  Zhiqiang Shen,et al.  QCM immunosensor detection of Escherichia coli O157:H7 based on beacon immunomagnetic nanoparticles and catalytic growth of colloidal gold. , 2011, Biosensors & bioelectronics.

[3]  Alphus D. Wilson,et al.  Applications and Advances in Electronic-Nose Technologies , 2009, Sensors.

[4]  Yuan Jiang,et al.  Application of real-time PCR for quantitative detection of Campylobacter jejuni in poultry, milk and environmental water. , 2003, FEMS immunology and medical microbiology.

[5]  R. Xiang,et al.  Loop-mediated isothermal amplification method targets to the phoP gene for detection of Yersinia enterocolitica. , 2010, Molecular and cellular probes.

[6]  Naresh Magan,et al.  Milk-sense: a volatile sensing system recognises spoilage bacteria and yeasts in milk , 2001 .

[7]  K. Holmstrøm,et al.  Inhibition of PCR by components of food samples, microbial diagnostic assays and DNA-extraction solutions. , 1992, International journal of food microbiology.

[8]  María Pedrero,et al.  Sensitive and rapid amperometric magnetoimmunosensor for the determination of Staphylococcus aureus , 2012, Analytical and Bioanalytical Chemistry.

[9]  Alisa Rudnitskaya,et al.  Evaluation of a novel chemical sensor system to detect clinical mastitis in bovine milk. , 2007, Biosensors & bioelectronics.

[10]  Guicheng Huo,et al.  DEVELOPMENT AND EVALUATION OF A LOOP‐MEDIATED ISOTHERMAL AMPLIFICATION (LAMP) METHOD FOR DETECTING LISTERIA MONOCYTOGENES IN RAW MILK , 2010 .

[11]  Paula García-Nogales,et al.  Comparison of commercially-available RNA extraction methods for effective bacterial RNA isolation from milk spiked samples , 2010 .

[12]  P. Brignon,et al.  Direct Detection of Viable Bacteria, Molds, and Yeasts by Reverse Transcriptase PCR in Contaminated Milk Samples after Heat Treatment , 1998, Applied and Environmental Microbiology.

[13]  Thusitha S. Gunasekera,et al.  A Flow Cytometry Method for Rapid Detection and Enumeration of Total Bacteria in Milk , 2000, Applied and Environmental Microbiology.

[14]  Giorgio Brandi,et al.  Direct detection of Listeria monocytogenes from milk by magnetic based DNA isolation and PCR , 2004 .

[15]  E. Alocilja,et al.  Market analysis of biosensors for food safety. , 2003, Biosensors & bioelectronics.

[16]  B. Ye,et al.  Multiplexed Bead-Based Mesofluidic System for Detection of Food-Borne Pathogenic Bacteria , 2009, Applied and Environmental Microbiology.

[17]  A M Walker,et al.  Verotoxin producing Escherichia coli O 157 infections associated with the consumption of yoghurt , 1993, Epidemiology and Infection.

[18]  Yanbin Li,et al.  Interdigitated microelectrode (IME) impedance sensor for the detection of viable Salmonella typhimurium. , 2004, Biosensors & bioelectronics.

[19]  R. Xiang,et al.  A loop-mediated isothermal amplification method targets the phoP gene for the detection of Salmonella in food samples. , 2009, International journal of food microbiology.

[20]  I. Biunno,et al.  Technical note: Improved method for rapid DNA extraction of mastitis pathogens directly from milk. , 2006, Journal of dairy science.

[21]  J. Lejeune,et al.  Food safety: unpasteurized milk: a continued public health threat. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[22]  Aída Juliana Martínez,et al.  Detection of Listeria monocytogenes in raw whole milk for human consumption in Colombia by real-time PCR , 2009 .

[23]  David J Beebe,et al.  Facile and rapid DNA extraction and purification from food matrices using IFAST (immiscible filtration assisted by surface tension). , 2012, The Analyst.

[24]  Olivier Lazcka,et al.  Pathogen detection: a perspective of traditional methods and biosensors. , 2007, Biosensors & bioelectronics.

[25]  Khalil Arshak,et al.  An overview of foodborne pathogen detection: in the perspective of biosensors. , 2010, Biotechnology advances.

[26]  A. Pinder,et al.  Detection of Salmonella typhimurium in dairy products with flow cytometry and monoclonal antibodies , 1994, Applied and environmental microbiology.

[27]  Nobuyasu Yamaguchi,et al.  Rapid On-chip flow Cytometric Detection of Listeria monocytogenes in Milk , 2009 .

[28]  H. Tsen,et al.  Combination of immunomagnetic separation and polymerase chain reaction for the simultaneous detection of Listeria monocytogenes and Salmonella spp. in food samples. , 2001, Journal of food protection.

[29]  Murat O. Balaban,et al.  Microbial and Sensory Assessment of Milk with an Electronic Nose , 2002 .

[30]  Y. Chuang,et al.  Disposable amperometric immunosensing strips fabricated by Au nanoparticles-modified screen-printed carbon electrodes for the detection of foodborne pathogen Escherichia coli O157:H7. , 2008, Biosensors & bioelectronics.

[31]  L. Slutsker,et al.  An outbreak of Yersinia enterocolitica O:8 infections associated with pasteurized milk. , 2000, The Journal of infectious diseases.

[32]  F. Allerberger,et al.  Outbreak of staphylococcal food intoxication after consumption of pasteurized milk products, June 2007, Austria , 2008, Wiener klinische Wochenschrift.

[33]  Joseph Maria Kumar Irudayaraj,et al.  Direct detection of E. Coli O157:H7 in selected food systems by a surface plasmon resonance biosensor , 2007 .

[34]  M. Wagner,et al.  Real-time PCR for the detection of Salmonella spp. in food: An alternative approach to a conventional PCR system suggested by the FOOD-PCR project. , 2006, Journal of microbiological methods.

[35]  Steven Ripp,et al.  Bacteriophage reporter technology for sensing and detecting microbial targets , 2011, Analytical and bioanalytical chemistry.

[36]  Timothy M. Chinowsky,et al.  Performance of the Spreeta 2000 integrated surface plasmon resonance affinity sensor , 2003 .

[37]  M. Brasca,et al.  A DNA array based assay for the characterization of microbial community in raw milk. , 2009, Journal of microbiological methods.

[38]  Peter Rossmanith,et al.  Detection of Listeria monocytogenes in food using a combined enrichment/real-time PCR method targeting the prfA gene. , 2006, Research in microbiology.

[39]  Jun Wang,et al.  Monitoring of quality and storage time of unsealed pasteurized milk by voltammetric electronic tongue , 2013 .

[40]  María Pedrero,et al.  Electrochemical immunosensor designs for the determination of Staphylococcus aureus using 3,3-dithiodipropionic acid di(N-succinimidyl ester)-modified gold electrodes , 2008 .

[41]  S. Riyaz-Ul-Hassan,et al.  Real‐time PCR‐based rapid and culture‐independent detection of Salmonella in dairy milk – addressing some core issues , 2013, Letters in applied microbiology.

[42]  Yin Liu,et al.  SENSITIVE AND RAPID DETECTION OF ENTEROBACTER SAKAZAKII IN INFANT FORMULA BY LOOP‐MEDIATED ISOTHERMAL AMPLIFICATION METHOD , 2009 .

[43]  Rashid Bashir,et al.  Electrical/electrochemical impedance for rapid detection of foodborne pathogenic bacteria. , 2008, Biotechnology advances.

[44]  Mickaël Boyer,et al.  Analytical opportunities of quantitative polymerase chain reaction in dairy microbiology , 2013 .

[45]  Giorgio Brandi,et al.  A new platform for Real-Time PCR detection of Salmonella spp., Listeria monocytogenes and Escherichia coli O157 in milk. , 2009, Food microbiology.

[46]  H. Falentin,et al.  Specific metabolic activity of ripening bacteria quantified by real-time reverse transcription PCR throughout Emmental cheese manufacture. , 2010, International journal of food microbiology.

[47]  Y. Chiang,et al.  Development of potency assays for a plasmid containing vascular endothelial growth factor 2 , 2010 .

[48]  A. Ozcan,et al.  Quantum dot enabled detection of Escherichia coli using a cell-phone. , 2012, The Analyst.

[49]  J. Compton,et al.  Nucleic acid sequence-based amplification , 1991, Nature.

[50]  Ihab Abdel-Hamid,et al.  Detection of pathogenic bacteria in food samples using highly-dispersed carbon particles. , 2005, Biosensors & bioelectronics.

[51]  M. Pividori,et al.  Rapid detection of Salmonella in milk by electrochemical magneto-immunosensing. , 2009, Biosensors & bioelectronics.

[52]  Terry J. Smith,et al.  tmRNA--a novel high-copy-number RNA diagnostic target--its application for Staphylococcus aureus detection using real-time NASBA. , 2009, FEMS microbiology letters.

[53]  Craig A. Grimes,et al.  Theory, Instrumentation and Applications of Magnetoelastic Resonance Sensors: A Review , 2011, Sensors.

[54]  W. Horwitz,et al.  Official methods of analysis of AOAC International , 2010 .

[55]  H. Falentin,et al.  RNA extraction from cheese for analysis of in situ gene expression of Lactococcus lactis , 2008, Journal of applied microbiology.

[56]  S. Doyle,et al.  PCR‐ELISA detection of Escherichia coli in milk , 2002, Letters in applied microbiology.

[57]  K. Takeuchi,et al.  Persistence of Escherichia coli O157:H7 in dairy fermentation systems. , 1998, Journal of Food Protection.

[58]  B. Chin,et al.  Magnetoelastic biosensor for the detection of Salmonella typhimurium in food products , 2007 .

[59]  M. Magnani,et al.  Development of a magnetic capture hybridization‐PCR assay for Listeria monocytogenes direct detection in milk samples , 2006, Journal of applied microbiology.

[60]  Rashid Bashir,et al.  On-chip parallel detection of foodborne pathogens using loop-mediated isothermal amplification , 2013, Biomedical Microdevices.

[61]  Huangxian Ju,et al.  A Rapid and Sensitive Aptamer-Based Electrochemical Biosensor for Direct Detection of Escherichia Coli O111 , 2012 .

[62]  Jeffrey D. Brewster,et al.  Detection and quantitation of Escherichia coli O157 in raw milk by direct qPCR , 2013 .

[63]  H. Heine,et al.  Acinetobacter lwoffii and Lactococcus lactis strains isolated from farm cowsheds possess strong allergy-protective properties. , 2007, The Journal of allergy and clinical immunology.

[64]  Frances S Ligler,et al.  Multiplexed magnetic microsphere immunoassays for detection of pathogens in foods , 2010, Sensing and instrumentation for food quality and safety.

[65]  G. Pershagen,et al.  Environmental bacteria and childhood asthma , 2012, Allergy.

[66]  G G Guilbault,et al.  Increasing the sensitivity of Listeria monocytogenes assays: evaluation using ELISA and amperometric detection. , 1999, The Analyst.

[67]  Suk-Ho Choi,et al.  Development of Reverse Transcriptase-polymerase Chain Reaction of fimA Gene to Detect Viable Salmonella in Milk , 2004 .

[68]  Burkhard Malorny,et al.  Comparison of PCR-ELISA and LightCycler real-time PCR assays for detecting Salmonella spp. in milk and meat samples. , 2004, Molecular and cellular probes.

[69]  Florence Postollec,et al.  Recent advances in quantitative PCR (qPCR) applications in food microbiology. , 2011, Food microbiology.

[70]  A. Merkoçi,et al.  Nanomaterials based biosensors for food analysis applications , 2011 .

[71]  P. Mandal,et al.  Methods for Rapid Detection of Foodborne Pathogens: An Overview , 2011 .

[72]  Joseph Maria Kumar Irudayaraj,et al.  Rapid detection of Salmonella enteritidis and Escherichia coli using surface plasmon resonance biosensor , 2006 .

[73]  H. Tsen,et al.  Use of tuf gene-based primers for the PCR detection of probiotic Bifidobacterium species and enumeration of bifidobacteria in fermented milk by cultural and quantitative real-time PCR methods. , 2010, Journal of food science.

[74]  J. Coia,et al.  Outbreak of Escherichia coli 0157 infection associated with pasteurised milk supply , 1994, The Lancet.

[75]  B Dufour,et al.  Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. , 2001, International journal of food microbiology.

[76]  Peter Ertl,et al.  Microfluidic Systems for Pathogen Sensing: A Review , 2009, Sensors.

[77]  Bryan A. Chin,et al.  Detection of Salmonella typhimurium in fat free milk using a phage immobilized magnetoelastic sensor , 2007 .

[78]  C. Holm,et al.  A Flow-Cytometric Gram-Staining Technique for Milk-Associated Bacteria , 2003, Applied and Environmental Microbiology.

[79]  H. Tsen,et al.  Development and use of tuf gene-based primers for the multiplex PCR detection of Lactobacillus acidophilus, Lactobacillus casei group, Lactobacillus delbrueckii, and Bifidobacterium longum in commercial dairy products. , 2009, Journal of food protection.

[80]  Hyang-Mi Nam,et al.  Application of SYBR green real-time PCR assay for specific detection of Salmonella spp. in dairy farm environmental samples. , 2005, International journal of food microbiology.

[81]  D. Hunter,et al.  Rapid and Sensitive Detection of Mycobacterium avium subsp. paratuberculosis in Bovine Milk and Feces by a Combination of Immunomagnetic Bead Separation-Conventional PCR and Real-Time PCR , 2004, Journal of Clinical Microbiology.

[82]  M. Peris,et al.  Review: highlights in recent applications of electronic tongues in food analysis. , 2010, Analytica chimica acta.

[83]  Ming-Che Wu,et al.  Development of a Novel Biochip for Rapid Multiplex Detection of Seven Mastitis-Causing Pathogens in Bovine Milk Samples , 2008, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[84]  J. Oliver,et al.  Recent findings on the viable but nonculturable state in pathogenic bacteria. , 2010, FEMS microbiology reviews.

[85]  D. Veal,et al.  Potential for broad applications of flow cytometry and fluorescence techniques in microbiological and somatic cell analyses of milk. , 2003, International journal of food microbiology.

[86]  Detlef Snakenborg,et al.  Improved bacteria detection by coupling magneto-immunocapture and amperometry at flow-channel microband electrodes. , 2011, Biosensors & bioelectronics.

[87]  J. Riu,et al.  Real-time potentiometric detection of bacteria in complex samples. , 2010, Analytical chemistry.

[88]  Jeong-Yeol Yoon,et al.  Lab-on-a-Chip Pathogen Sensors for Food Safety , 2012, Sensors.

[89]  O. Stephansson,et al.  AUTOMATED BACTERIAL DNA ISOLATION FROM FOOD AND FEED SAMPLES – A BIOPREPAREDNESS DESIGN , 2011 .

[90]  Lee-Ann Jaykus,et al.  Bacterial Separation and Concentration from Complex Sample Matrices: A Review , 2004, Critical reviews in microbiology.

[91]  John G. Bruno,et al.  Plastic-Adherent DNA Aptamer-Magnetic Bead and Quantum Dot Sandwich Assay for Campylobacter Detection , 2009, Journal of Fluorescence.

[92]  T. H. Rider,et al.  A B Cell-Based Sensor for Rapid Identification of Pathogens , 2003, Science.

[93]  Orla O'Sullivan,et al.  The complex microbiota of raw milk. , 2013, FEMS microbiology reviews.

[94]  Michael Keusgen,et al.  Rapid method for detection of Salmonella in milk by surface plasmon resonance (SPR). , 2007, Biosensors & bioelectronics.

[95]  Nobuyasu Yamaguchi,et al.  Rapid detection of respiring Escherichia coli O157:H7 in apple juice, milk, and ground beef by flow cytometry , 2003, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[96]  Choi Jeong-Woo,et al.  Lab-on-a-chip for monitoring the quality of raw milk , 2006 .

[97]  I. Grant,et al.  Detection by immunomagnetic PCR of Mycobacterium avium subsp. paratuberculosis in milk from dairy goats in Norway. , 2003, Veterinary microbiology.

[98]  C. Rodriguez-Emmenegger,et al.  Poly(HEMA) brushes emerging as a new platform for direct detection of food pathogen in milk samples. , 2011, Biosensors & bioelectronics.

[99]  K. Asano,et al.  A real-time PCR method targeting a gene sequence encoding 16S rRNA processing protein, rimM, for detection and enumeration of Streptococcus thermophilus in dairy products. , 2009 .